Impaired Corollary Discharge in Psychosis and At-Risk States: Integrating Neurodevelopmental, Phenomenological, and Clinical Perspectives

Abstract

The brain is increasingly viewed in contemporary neuroscience as a predictive machine; its products, such as movements and decisions, are indeed accompanied by predictions of outcomes at distinct levels of awareness. In this conceptual review, we focus on corollary discharge, a basic neurophysiological mechanism that is allegedly involved in sensory prediction and contributes to the distinction between self-generated and externally generated actions. Failures in corollary discharge have been hypothesized as potentially relevant for the progressive development of positive psychotic symptoms such as passivity delusions and auditory verbal hallucinations. We articulate this framework adopting three confocal lenses, namely, the neurodevelopmental, phenomenological, and clinical perspectives. Converging evidence from these research domains indicates a possible developmental cascade leading to increased lifetime risk of psychosis. That is, early childhood alterations of corollary discharge mechanisms, endophenotypically expressed in motor impairment, may concur with a progressive fading of the feeling of self-agency on one's own experiences. Combined with other age-dependent situational challenges occurring along development, this may progressively hamper the ontogenesis of the embodied self, thereby facilitating the emergence of anomalous subjective experiences such as self-disorders (a longitudinal index of schizophrenia spectrum vulnerability) and broadly conceived clinical high-risk states. Overall, this condition increases the risk of developing passivity symptoms, phenotypically expressed in a severity gradient ranging from intrusive thoughts to passivity delusions and auditory verbal hallucinations. Empirical and clinical implications of this framework, as well as future scenarios, are discussed.

Keywords: Corollary discharge; Obsessive-compulsive disorder; Schizophrenia spectrum disorders; Self-disorders; Sense of agency; Sensory prediction.